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Muscle force regulates bone shaping for optimal load-bearing capacity during embryogenesis.

Abstract The vertebrate skeleton consists of over 200 individual bones, each with its own unique shape, size and function. We study the role of intrauterine muscle-induced mechanical loads in determining the three-dimensional morphology of developing bones. Analysis of the force-generating capacity of intrauterine muscles in mice revealed that developing bones are subjected to significant and progressively increasing mechanical challenges. To evaluate the effect of intrauterine loads on bone morphogenesis and the contribution of the emerging shape to the ability of bones to withstand these loads, we monitored structural and mineral changes during development. Using daily micro-CT scans of appendicular long bones we identify a developmental program, which we term preferential bone growth, that determines the specific circumferential shape of each bone by employing asymmetric mineral deposition and transient cortical thickening. Finite element analysis demonstrates that the resulting bone structure has optimal load-bearing capacity. To test the hypothesis that muscle forces regulate preferential bone growth in utero, we examine this process in a mouse strain (mdg) that lacks muscle contractions. In the absence of mechanical loads, the stereotypical circumferential outline of each bone is lost, leading to the development of mechanically inferior bones. This study identifies muscle force regulation of preferential bone growth as the module that shapes the circumferential outline of bones and, consequently, optimizes their load-bearing capacity during development. Our findings invoke a common mechanism that permits the formation of different circumferential outlines in different bones.
PMID
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Authors

Mayor MeshTerms
Keywords
Journal Title development (cambridge, england)
Publication Year Start




PMID- 21750035
OWN - NLM
STAT- MEDLINE
DCOM- 20110919
LR  - 20110713
IS  - 1477-9129 (Electronic)
IS  - 0950-1991 (Linking)
VI  - 138
IP  - 15
DP  - 2011 Aug
TI  - Muscle force regulates bone shaping for optimal load-bearing capacity during
      embryogenesis.
PG  - 3247-59
LID - 10.1242/dev.063768 [doi]
AB  - The vertebrate skeleton consists of over 200 individual bones, each with its own 
      unique shape, size and function. We study the role of intrauterine muscle-induced
      mechanical loads in determining the three-dimensional morphology of developing
      bones. Analysis of the force-generating capacity of intrauterine muscles in mice 
      revealed that developing bones are subjected to significant and progressively
      increasing mechanical challenges. To evaluate the effect of intrauterine loads on
      bone morphogenesis and the contribution of the emerging shape to the ability of
      bones to withstand these loads, we monitored structural and mineral changes
      during development. Using daily micro-CT scans of appendicular long bones we
      identify a developmental program, which we term preferential bone growth, that
      determines the specific circumferential shape of each bone by employing
      asymmetric mineral deposition and transient cortical thickening. Finite element
      analysis demonstrates that the resulting bone structure has optimal load-bearing 
      capacity. To test the hypothesis that muscle forces regulate preferential bone
      growth in utero, we examine this process in a mouse strain (mdg) that lacks
      muscle contractions. In the absence of mechanical loads, the stereotypical
      circumferential outline of each bone is lost, leading to the development of
      mechanically inferior bones. This study identifies muscle force regulation of
      preferential bone growth as the module that shapes the circumferential outline of
      bones and, consequently, optimizes their load-bearing capacity during
      development. Our findings invoke a common mechanism that permits the formation of
      different circumferential outlines in different bones.
FAU - Sharir, Amnon
AU  - Sharir A
AD  - Department of Molecular Genetics, Weizmann Institute of Science, Rehovot 76100,
      Israel.
FAU - Stern, Tomer
AU  - Stern T
FAU - Rot, Chagai
AU  - Rot C
FAU - Shahar, Ron
AU  - Shahar R
FAU - Zelzer, Elazar
AU  - Zelzer E
LA  - eng
PT  - Journal Article
PT  - Research Support, Non-U.S. Gov't
PL  - England
TA  - Development
JT  - Development (Cambridge, England)
JID - 8701744
SB  - IM
MH  - Adaptation, Physiological/physiology
MH  - Animals
MH  - Bone Density/physiology
MH  - Bone and Bones/*anatomy & histology/*physiology
MH  - Embryo, Mammalian/*anatomy & histology/*physiology
MH  - Embryonic Development/*physiology
MH  - Female
MH  - Male
MH  - Mice
MH  - Mice, Inbred C57BL
MH  - Muscle Contraction/physiology
MH  - Muscle, Smooth/physiology
MH  - Periosteum/cytology/growth & development
MH  - Pregnancy
MH  - Stress, Mechanical
MH  - Uterus/anatomy & histology/physiology
MH  - Weight-Bearing/*physiology
EDAT- 2011/07/14 06:00
MHDA- 2011/09/20 06:00
CRDT- 2011/07/14 06:00
PHST- 2011/07/14 06:00 [entrez]
PHST- 2011/07/14 06:00 [pubmed]
PHST- 2011/09/20 06:00 [medline]
AID - 138/15/3247 [pii]
AID - 10.1242/dev.063768 [doi]
PST - ppublish
SO  - Development. 2011 Aug;138(15):3247-59. doi: 10.1242/dev.063768.